How Are Endemic and Widely Distributed Bromeliads Responding To

Flora 238 (2018) 110–118

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How are endemic and widely distributed bromeliads responding to

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warming temperatures? A case study in a Brazilian hotspot

∗,1 1 ∗

Cleber Juliano Neves Chaves , Bárbara Simões Santos Leal , José Pires de Lemos-Filho

Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: The increase in mean global temperature is causing extensive changes in ecosystems. However, little

Received 26 December 2016

is yet known about the heat tolerance of neotropical plant species. Here, we investigate heat tolerance

Received in revised form 10 May 2017

variation in both restricted and widely distributed bromeliad species co-occurring in campo rupestre, a

Accepted 13 May 2017

megadiverse ecosystem in central and eastern Brazil. We determined the heat tolerance of the photo-

Edited by P. Morellato

synthetic apparatus using chlorophyll ﬂuorescence measurements to test if the endemic species Vriesea

Available online 25 May 2017

minarum is more heat sensitive than two widely distributed species, Vriesea bituminosa and Aechmea

nudicaulis. Furthermore, we tested if the distinct photosynthetic metabolisms of the species, sun expo-

Keywords:

sure, and rainfall seasonality of campo rupestre inﬂuence this outcome. Our results show that, contrary

Thermal tolerance

to our expectations, the endemic campo rupestre species did not show the greatest heat sensitivity, but

Climate change

Bromeliaceae did have one of the lowest heat tolerance plasticities. The CAM bromeliad A. nudicaulis was more heat

Species range tolerant than the other bromeliad species, but both heat tolerance and its plasticity are highly affected by

CAM sun exposure and the rainfall seasonality of campo rupestre. The low values and plasticity of V. minarum

3 thermal tolerance could indicate that the threat of global warming could be greater for this campo rupestre

endemic species. Our results also indicate that heat tolerance, especially the ability to withstand stressful

temperatures for a long time, is an important parameter that differentiates the ecological strategies of

these bromeliads species.

1. Introduction plasticity); developing new evolutionary strategies; changing their

abundance and inter-speciﬁc interactions; and shifting their distri-

◦ ◦

Temperatures below 10 C and above 35 C can cause perma- bution (Holt, 1990; Parmesan, 2006; Blois et al., 2013; IPCC, 2014;

nent damages to most plants (Went, 1953; Berry and Bjorkman, Parmesan and Hanley, 2015). Studies have suggested, for instance,

1980). The rise in the mean global temperature observed over the that some species have become restricted to refuges (see Rull, 2009;

◦

last century (IPCC, 2007) and an increase of ca. 2 C in the maxi- Stewart et al., 2010), shifting their ranges poleward and toward

mum global temperature during the ﬁrst half of the 21 st century higher elevations due to the warming temperatures since the last

(IPCC, 2012) are causing deep alterations to ecosystems, from dam- glacial maximum (LGM; e.g., Parmesan and Yohe, 2003; Root et al.,

ages to the chloroplast integrity of plants (Berry and Bjorkman, 2003; Parmesan, 2006; Colwell et al., 2008; Rosenzweig et al., 2008;

1980; Yamane et al., 2000; Hüve et al., 2011; Zhang et al., 2012) Chen et al., 2011; Bässler et al., 2013; Pecl et al., 2017). Thus, species

to mass extinctions (e.g. Crowley and North, 1987; Malcolm et al., currently restricted to interglacial refuges may be more sensitive

2006; Carpenter et al., 2008; Weigelt et al., 2016). But prior to to warming temperatures than widely distributed species.

going extinct, species may respond to climate change by altering Due to its past climatic stability, the campo rupestre ecosystem

their phenology and other physiological responses (i.e. phenotypic represents an example of interglacial refuge in the Neotropics (Bon-

atelli et al., 2014; Barbosa et al., 2015). This vegetation complex

is endemic to Brazil, and it is usually restricted to altitudes from

900 to over 2,000 ma.s.l., forming a mosaic archipelago-like system

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on low water-holding rocks of mountaintops surrounded by low-

This article is part of a special issue entitled Plant life in campo rupestre: new

lessons from an ancient biodiversity hotspot published at the journal FLORA 238C. lands (Alves et al., 2014; Silveira et al., 2016). Studies have shown ∗

Corresponding authors.

that campo rupestre is probably the most ancient open vegetation

E-mail addresses: [email protected] (C.J.N. Chaves),

in eastern South America, comprising a great diversity and rate of

[email protected] (B.S.S. Leal), [email protected] (J.P.d. Lemos-Filho).

1 endemism (Alves et al., 2014; Silveira et al., 2016). Nevertheless,

Departamento de Ecologia, Instituto de Biociências, Universidade Estadual

Paulista, São Paulo, Rio Claro, Brazil. recent studies indicate that campo rupestre vegetation could lose

https://doi.org/10.1016/j.ﬂora.2017.05.003

C.J.N. Chaves et al. / Flora 238 (2018) 110–118 111

from 44% (Bitencourt et al., 2016) to 95% (Fernandes et al., 2012) 2014a, 2014b). Therefore, it remains unclear how these plants will

of its current area and about 25% of its angiosperm species due respond to ongoing climate change.

to climate change (Bitencourt et al., 2016). Such reduction repre- Inferences about potential responses of species to climate

sents the extinction of more than 400 microendemic plant species change from their current distribution can be a good strategy, since

which are currently restricted to future unsuitable areas (Biten- some works report a strong relationship between ecological char-

court et al., 2016). Such potential scenario is a consequence of the acteristics and niche projections (e.g. Thuiller et al., 2005; Garcia

◦

habitat reduction caused by a warming up to 5 C in temperature et al., 2014). Here, we aim to test whether an endemic bromeliad

and an increase in frequency of extremely dry seasons. The low dis- species of campo rupestre is more sensitive to warming tempera-

persal ability of most endemic species makes them unable to reach tures than species with wider distributions. For such, we measured

other suitable mountains; and their high specialization level make the ﬂuorescence of photosystem II through two methods: ramping

them more sensitive to climate changes (Christensen et al., 2007; and static temperature assays. We also examine whether morpho-

Dawson et al., 2011; Bittencourt et al., 2016). Despite these wor- physiological traits, such as photosynthetic pathways (i.e., CAM and

rying forecasts, little is known about how these endemic species C3 photosynthesis), sun exposure, and the marked rainfall season-

would respond to overcome the warming temperatures. ality of the campo rupestre, can bias the outcome. Finally, we test

Bromeliaceae is one of the most representative plant families in whether heat tolerance and its plasticity can distinguish the eco-

campo rupestre and nearly half of the bromeliad species occurring logical strategies of these bromeliads.

in such environment are endemic (Versieux et al., 2008; Silveira

et al., 2016). This family is also one of the best examples of adap-

tive radiation in the Neotropics (Benzing, 2000; Givnish et al., 2. Material and methods

2014; Givnish, 2015; Palma-Silva et al., 2016). Crassulacean acid

metabolism (CAM), for example, is often noted as a key innovation 2.1. Study site and plant species

in the family that allowed the exploitation of arid environments,

due to its mechanism that closes the stomata during the daytime This study was carried out in the Piedade Mountains (Serra da

and avoids excessive water loss during dry periods (Givnish et al., Piedade), situated within the over-exploited Iron Quadrangle, in

2014; Silvestro et al., 2014; Palma-Silva et al., 2016). Global cli- the southern-most section of the core area of the campo rupestre

matic changes may favor species with CAM metabolism, due to in the Espinhac¸ o Range, Eastern Brazil (Alves et al., 2014; Silveira

their supposed higher thermal tolerance (e.g., Yamada et al., 1996; et al., 2016). The Piedade Mountains have a maximum altitude of

Weng and Lai, 2005) and the anthropogenic increase of arid areas 1,746 ma.s.l., and the highest section presents a typical subtropi-

(Nobel, 1988; Cushman and Borland, 2002; Mercier and Freschi, cal high-altitude climate, with a well-deﬁned dry season between

2008; Osmond et al., 2008). However, Chaves et al. (2015) showed April and September, and the frequent occurrence of fog (Brandão

that the daily organic acid accumulation of CAM plants has a strong and Gavilanes, 1990; Marques and Lemos-Filho, 2008). The sur-

negative impact on their thermal tolerance (see also Yamori et al., roundings (Belo Horizonte city, 40 km from Serra da Piedade) show

◦

a well-deﬁned dry season with an average temperature of 19 C

and 6 mm of precipitation in the driest month, and a well-deﬁned

Fig. 1. Schematic representation of the distribution of Aechema nudicaulis, Vriesea bituminosa, and Vriesea minarum according the online database of the Global Biodiversity

Information Facility (GBIF; via www.gbif.org).

112 C.J.N. Chaves et al. / Flora 238 (2018) 110–118

◦

wet season, with an average temperature of 23 C and 322 mm

of total precipitation in average on the wettest month (histori-

cal data from January 1990 to December 2016 achieved in the

◦

website www.inmet.gov.br). Frosts and temperatures close to 0 C

are common at the highest altitudes (Brandão and Gavilanes,

1990). Our study area is above 1,400 ma.s.l. and comprises two

microenvironments: a xeric zone, highly exposed to sun and winds,

characterized by the occurrence of iron-quartzite rock outcrops

and herbaceous-shrubby vegetation (hereafter referred to as sun-

exposed environment); and a shaded zone within an altitudinal

cloud forest, characterized by the presence of shrubby and arboreal

vegetation and high moisture (hereafter, shaded environment).

Here, we selected three bromeliad species: two C3 species,

Vriesea minarum L.B. Sm and Vriesea bituminosa Wawra, from the

Tillandsioideae subfamily, and a CAM species, Aechmea nudicaulis

(L.) Griseb., from the Bromelioideae subfamily. Vriesea minarum is

a rupicolous species endemic to the campo rupestre (Fig. 1; Forzza

et al., 2012), occurring in sun-exposed environments of the Piedade

Mountains. Vriesea bituminosa occurs as a rupicolous or epiphytic

bromeliad in sections of forests associated with outcrops in eastern

Brazil and in Venezuela (Fig. 1; Coser, 2008; Forzza et al., 2012). At

the study site, this species is often found in shaded areas, where

we collected all samples. The CAM species, A. nudicaulis, is widely

distributed throughout the Neotropics, from Mexico to Peru, the

Caribbean, eastern Brazil, and Guyana (Fig. 1; Smith and Downs,

1979). In Brazil, the species occurs in sandy coastal zones, moist

forests, rock outcrops in the Atlantic Forest, and campos rupestres

(Bert and Luther, 2005). In our study site, A. nudicaulis were sam-

pled in both sun-exposed and shaded environments, designated

as “sun-exposed A. nudicaulis” and “shaded A. nudicaulis”, respec-

tively.

2.2. Microclimatic information

Fig. 2. Photosynthetic photon ﬂux density (PPFD) and average temperature of a day

in the dry (A) and rainy seasons (B). Full and dashed bars represent the PPFD of

To measure the seasonal climate differences of the study site, we shaded and exposed environments, respectively. Solid and dashed lines represent,

respectively, the temperature of shaded and exposed environments. The dotted line,

recorded photosynthetic photon ﬂux density (PPFD) and air tem-

in A, represents the temperature of rock outcrop.

perature data from sun-exposed and shaded environments on all

sampling days during the dry and rainy seasons (Fig. 2). We also

measured relative humidity in the shaded environment and the

dry-season surface temperature of a sun-exposed rocky outcrop. All

measurements were made using sensors coupled with data loggers

the collected samples in a hermetically sealed plastic bag and kept it

(LI-1400, LI-COR Inc. and TD-880, ICEL).

under natural light, partially shaded, for 24 h. We proceeded with

a thermal tolerance test in the laboratory, using an ex vivo pro-

2.3. Sampling

cedure. Previous tests of this procedure have shown that it does

not signiﬁcantly inﬂuence the measured potential quantum yield

We employed two different methods to determine photosyn-

(variable ﬂuorescence/maximum ﬂuorescence; F /F ) of the leaves

thetic thermal tolerance of the studied species: a ramping assay v m

(data not shown). Subsequently, we removed the samples from the

(under increasing temperatures) and a static assay (under constant

plastic bags and kept them in the dark and at room temperature

high temperature; see following sections). For the ramping assay,

∼ ◦

2 ( 25 C) for 15 min; we then measured the initial F /F using a

we collected ∼1.5 cm leaf samples from the top (upper third) and v m

modulate ﬂuorometer (MINI-PAM, Walz). The thermal tolerance

basal (bottom third) sections of one young and totally expanded

test was conducted as described by Godoy et al. (2011), but using a

leaf from ﬁve individuals of each studied group (sun-exposed A.

thermostatic water bath as a heater (214D2, QUIMIS). We sealed the

nudicaulis, shaded A. nudicaulis, V. minarum, and V. bituminosa).

aluminum plate containing the samples with a plastic bag and used

We sampled these individuals during the dry and rainy seasons,

a thermocouple linked to a digital thermometer (TD-880, ICEL) to

at 08:00 and 15:00, when organic acids reach their maximum and

check the temperature of samples. Leaf samples were subjected to

minimum accumulations in A. nudicaulis (due to CAM photosyn-

◦

increasing temperatures, from 35 C—the upper limit of the opti-

thesis; data not shown). We also sampled the same individuals

mal temperature range for most plants (Went, 1953; Berry and

to determine morphophysiological traits (see section 2.6). For the

◦ ◦

2 Bjorkman, 1980)—to 65 C, with an average increase of 1 C every

static assay, we collected ∼1.5 cm samples from the top and basal

◦

3 min. We measured F /F once after every increase of 2 C. The

leaf regions of ﬁve individuals from each studied group during the v m

data were used to determine the critical temperatures that pro-

rainy season, at 15:00; see follow sections).

mote a 15% (T15) and 50% (T50) reduction of the initial Fv/Fm, using

a sigmoidal equation (Fig. 3A) as described by Knight and Ackerly

2.4. Heat tolerance of photosystem II (PSII): ramping assay

(2003). This analysis was performed using a purpose-built function

in R statistical software version 3.0.1 (see Supplementary Material;

To determine the thermal tolerance of photosystem II (PsiI)

R Core Team, 2014).

under increasing temperatures (ramping assay), we placed each of

C.J.N. Chaves et al. / Flora 238 (2018) 110–118 113

Fig. 3. Schematic representation showing the Fv/Fm decrease (ﬁlled lines) under increasing temperature (A) and under time of exposure to a constant high temperature

◦

(43 C; B), highlighting the critical parameters (T15, T50, and D50). The dashed line in A represents the linear function of Fv/Fm decrease between T15 and T50. Shaded areas in

A and B represent, respectively, the temperature differences and the time elapsed between the decay of 15% and 50% on initial Fv/Fm.

Table 1

2.5. Heat tolerance of PSII: static assay

Means and standard errors of projected D50 values of all experimental groups at

15:00 in the rainy season. Same letters represent values statistically equal among

To test if the species most tolerant to increasing temperatures

all groups.

is also the most tolerant to constant stressful temperatures, we

Species Environment Leaf region D50 (min.)

followed an experimental procedure similar to the one described

above, except that the Fv/Fm measures were made before immers- A. nudicaulis Sun-exposed Top 80.86 11.8

Basal 103.17 ± 5.3

ing the samples in a water bath and again after 1, 5, 10, 20, 40, 60,

◦ Shaded Top 157.87 ± 17.4

and 80 min, at a constant temperature of 43 C (which represents a

Basal 163.66 ± 28.1

the average of T values obtained in the ramping assay for all the b

± 15 V. minarum Sun-exposed Top 73.19 4.8

samples of Vriesea species, the less heat tolerant groups; see Table Basal 81.56 ± 2.3

V. bituminosa Shaded Top 70.59 1.8

S1). We estimated the critical time, in minutes, that would promote

Basal 73.02 ± 0.9

a 50% reduction of the initial Fv/Fm (D50), using a linear function

(Fig. 3B). This analysis was also performed using a purpose-built

function in R statistical software version 3.0.1 (see Supplementary

2.7. Statistical analysis

Material; R Core Team, 2014).

We performed linear ﬁxed-effect models (LMEs) to test whether

the variation in thermal tolerance (T50, D50, and RDPIT50 values)

2.6. Morphophysiological traits and heat tolerance is associated with the measured morphophysiological traits, and

whether thermal tolerance and the morphophysiological traits are

To verify the relationships between heat tolerance and other related to each other, according Fig. 4A and 4B, respectively. We

morpho-physiological traits, and to distinguish the ecological used the explanatory variables as ﬁxed effects, and individual labels

strategies of each experimental group (sun-exposed A. nudicaulis, and their leaf regions as random variables. We tested the signif-

shaded A. nudicaulis, V. minarum, and V. bituminosa), we determined icance of the models through an analysis of variance (ANOVA),

the daily variation of titratable acidity (as per Hartsock and Nobel, sequentially removing all non-signiﬁcant variables (p > 0.05) with

1976), succulence index (SI; as per Ogburn and Edwards, 2010, the greatest p-values. To test if the plants with the highest ther-

2012), and relative water content (RWC) of all samples. Moreover, mal tolerance to increasing temperature are also the most thermal

we estimated the stomata and scale densities of the top and basal tolerant to static stressful temperatures, and to test whether both

sections of the leaves from each experimental group. To do this, assays are related, we performed a simple regression between T50

leaf samples were ﬁxed in FAA50 (Johansen, 1940) and stored in and D50 values of all studied groups.

ethanol 70% for subsequent analysis. The epidermises were excised Finally, we performed a canonical discriminant analysis (CDA)

by immersion in 66% commercial sodium hypochlorite for three followed by general linear models (GLM; see Fig. S1) to evaluate

days. We then stained the epidermises with safranin-astra blue whether thermal tolerance, together with the measured morpho-

(Bukatsch, 1972) and mounted them in Kaiser gelatin (Kraus and physiological variables, could discriminate the ecological strategies

Arduin, 1997). The adaxial and abaxial stomata and scales within of each species. All statistical analyses were performed with the

six 0.06-mm ﬁelds on each sample were counted using a micro- R packages “nlme”, “candisc”, and “glmulti” (Wagenmakers and

scope with a camera lucida (Stemi, 2000, Zeiss). We considered the Farrell, 2004; Friendly, 2007; Kenny and Hoyt, 2009).

scale density as the sum of both faces of each sample.

To overcome the variability of each physiological trait, we 3. Results

estimated the overall phenotypic plasticity based on the relative

distance phenotypic index (RDPI), as described by Valladares et al. 3.1. Heat tolerance of PSII

(2006). For each experimental group (sun-exposed A. nudicaulis,

shaded A. nudicaulis, V. minarum, and V. bituminosa), we calculated Generally, shaded Aechmea nudicaulis and Vriesea bituminosa

a combination of the relative distances between the values for these individuals showed the highest and the lowest heat tolerances,

traits for all collection times of day and seasons, generating only one respectively, under both ramping and static thermal tolerance

distance value. assays (Table 1, Fig. 4, and Tables S1 and S2). Considering the mean

114 C.J.N. Chaves et al. / Flora 238 (2018) 110–118

Fig. 4. Norms of reaction of T50 variations of sun-exposed (open squares) and shaded (closed squares) A. nudicaulis, V. minarum (open circles) and V. bituminosa (closed

triangles), between times of day in the dry (A) and rainy (B) seasons, and between seasons, at 08:00 (C) and 15:00 (D). Same letters represent no statistical differences

(p > 0.05). Each average showed also group the values of top and basal leaf sections of each individual.

of the T50 values of all studied groups, we found an interaction

among day times and seasons, with greater values at 15:00 in the

rainy season and lower values at 15:00 in the dry season (Fig. 4 and

Table S1). In the ramping assay performed in the morning, as well as

in the static assay, we detected a signiﬁcantly higher thermal toler-

ance in shaded A. nudicaulis than in sun-exposed plants, which had

a thermal tolerance similar to that of Vriesea species (Tables 1, and

S1). No signiﬁcant differences were detected between leaf regions

(p > 0.05; Table 1). We observed directly proportional relationships

between T50 and D50 (Fig. 5).

3.2. Morphophysiological traits and heat tolerance

The relationships between heat tolerance and morphophysi-

ological variables were signiﬁcant only for titratable acidity of

the basal leaf regions of A. nudicaulis sampled in the rainy sea-

son. Titratable acidity was inversely proportional to the T50 values

(Fig. 6). Regarding the plasticity of morphophysiological traits,

Fig. 5. Exponential relationship between T50 (ramping assay) and D50 (static assay)

sun-exposed A. nudicaulis showed some of the greatest signiﬁcant

values of all studied groups obtained during the rainy season at 15:00.

values for most of them, except for Titratable acidity and SI in the

top and basal leaf regions, respectively (Table 2). In these cases,

shaded A. nudicaulis was the most plastic. For most of the other ues, however, were not statistically distinct from the other studied

cases, shaded A. nudicaulis was, together with V. minarum, the less groups (Table S2). For stomata density, V. minarum and V. bitumi-

plastic group (Table 2). nosa had, respectively, the lowest and the highest absolute values

The top of sun-exposed A. nudicaulis leaves had the greatest among the top regions of the leaves (Table S3). For scale density,

daily variation of titratable acidity (H ; Table S2). Their SI val- V. minarum and V. bituminosa had, respectively, the lowest and the

C.J.N. Chaves et al. / Flora 238 (2018) 110–118 115

Table 3

Results of AICi (Akaike criterion for model i), i(AIC) (AICi − minAIC), and wi(AIC)

(rounded Akaike weights) for all competing models. Bold rows indicate the best ﬁt

models, based on i(AIC) <2.0.

Model AICi i(AIC) wi(AIC)

D50 + RDPI acidity + acidity + RDPI SI 18.280 0.000 5.26E-001

SI + D50 + RDPI acidity + acidity + RDPI SI 19.387 1.108 3.02E-001

D50 + RDPI acidity + acidity 21.997 3.718 8.20E-002

SI + D50 + RDPI acidity + acidity 23.303 5.024 4.27E-002

SI + D50 + acidity + RDPI SI 24.089 5.809 2.88E-002

RDPI acidity + acidity + RDPI SI 28.013 9.734 4.05E-003

D50 + acidity + RDPI SI 28.551 10.272 3.09E-003

SI + D50 + acidity 28.907 10.627 2.59E-003

RDPI acidity + acidity 29.038 10.759 2.43E-003

SI + RDPI acidity + acidity + RDPI SI 30.006 11.726 1.50E-003

acidity + RDPI SI 30.797 12.518 1.01E-003

D50 + acidity 30.927 12.647 9.43E-004

SI + RDPI acidity + acidity 31.025 12.745 8.98E-004

SI + acidity + RDPI SI 31.161 12.881 8.39E-004

acidity 32.549 14.269 4.19E-004

SI + acidity 33.985 15.705 2.05E-004

Fig. 6. Negative relationships between T50 and titratable acidity in basal region of

SI + D50 + RDPI acidity + RDPI SI 39.168 20.888 1.53E-005

sun-exposed (open diamond) and shaded (closed diamond) A. nudicaulis.

SI + D50 + RDPI SI 39.755 21.476 1.14E-005

SI + D50 + RDPI acidity 39.772 21.492 1.13E-005

SI + RDPI SI 41.875 23.596 3.96E-006

SI + D50 43.112 24.833 2.13E-006

SI + RDPI acidity + RDPI SI 43.451 25.172 1.80E-006

D50 + RDPI acidity 43.477 25.198 1.78E-006

D50 + RDPI acidity + RDPI SI 44.236 25.956 1.22E-006

RDPI acidity 44.839 26.559 8.99E-007

RDPI acidity + RDPI SI 45.042 26.763 8.12E-007

SI 45.116 26.836 7.83E-007

SI + RDPI acidity 45.275 26.995 7.23E-007

RDPI SI 46.300 28.020 4.33E-007

NULL 46.987 28.707 3.07E-007

D50 + RDPI SI 48.089 29.810 1.77E-007

D50 48.695 30.415 1.31E-007

S4). The second canonical axis — most associated with variation of

titratable acidity, D50 and the RDPI of SI — accounted for 18.1% of the

trait variation (Table S4) and differentiated sun-exposed A. nudi-

caulis from the other groups (Fig. 7). The best model to describe the

variances of discriminated functional groups (based on AIC < 2.0)

included the average of D50, the mean and RDPI of titratable acidity,

Fig. 7. Biplot representation of the scores on the ﬁrst two axes of the canonical

and the RDPI of SI (Table 3).

discriminant analysis for 13 morphophysiological variables of sun-exposed (open

squares) and shaded (closed squares) A. nudicaulis, V. minarum (open circles), and

V. bituminosa (closed triangles). The centroids of each group are represented by a

4. Discussion

cross.

Our results did not corroborate the hypothesis that the

highest absolute values in the basal regions of the leaves (Table bromeliad species restricted to the campo rupestre, Vriesea

S3). However, stomata and scale density of C3 species were not minarum, is more heat sensitive than the other studied species.

statistically distinct from those of A. nudicaulis (Table S3). Instead, we demonstrated that its heat tolerance was similar to the

The ecological strategies of each experimental group (sun- individuals of the most widely distributed species, Aechema nudi-

exposed A. nudicaulis, shaded A. nudicaulis, V. minarum, and V. caulis, growing under the same conditions of V. minarum. Despite

bituminosa) were clearly discriminated by CDA analysis (Fig. 7). The this result, V. minarum showed a low thermal tolerance plastic-

ﬁrst canonical axis accounted for 77.2% of trait variation and dis- ity that was statistically equal to those of shaded individuals of

criminated almost all studied groups (Fig. 7). This axis grouped the A. nudicaulis. On the other hand, the low thermal tolerance and

variation of mainly SI, D50, and the RDPI of titratable acidity (Table the plasticity of V. minarum indicate a great level of specializa-

Table 2

Mean of total plasticity index (RDPI) of T50, titratable acidity, SI and RWC of each experimental group. Same superscript letters represent values statistically equal between

all experimental groups, for each leaf region. Asterisks represent differences statistically signiﬁcant (p < 0.05) between leaf regions.

Parameter measured Leaf region Sun-exposed A. nudicaulis Shaded A. nudicaulis V. minarum V. bituminosa

a c bc b T50 Top 0.031 0.020 0.022 0.026 a c c b

Basal 0.038 0.024 0.021 0.031

b a b b

Titratable acidity Top 0.219 * 0.350 0.190 0.182

a b c c

Basal 0.410 * 0.310 0.208 0.219

a a a a

SI Top 0.119 * 0.116 * 0.101 0.119

c a c b

Basal 0.074 * 0.162 * 0.093 0.119

a b a a

RWC Top 0.125 0.058 * 0.111 * 0.137

a bc c ab

Basal 0.138 0.102 * 0.077 * 0.125

116 C.J.N. Chaves et al. / Flora 238 (2018) 110–118

tion of this species to the current conditions of campo rupestre, and daily variations observed for both physiological parameters dur-

the extra susceptibility of this species to climate change (see Vié ing the rainy season. This relationship was reported for other CAM

et al., 2009). Extrapolating these results and considering the high plants (Larcher, 1980; Lösch and Kappen, 1983; Kappen and Lösch,

endemism rate and specialization of campo rupestre species (see 1984; Krause et al., 2016) as well as for another CAM bromeliad,

Silveira et al., 2016), our results may presage a worrying scenario for which Chaves et al. (2015) showed that, under controlled con-

for this vegetation proﬁle under global warming. ditions, leaf acidity decreases and thermal tolerance increases as

The shaded individuals of A. nudicaulis showed the highest heat temperature increases. This mechanism may have evolved due to

tolerance among the studied groups. In fact, we found a wide varia- the increase in tonoplast permeability and acid remobilization from

tion in heat tolerance between sun-exposed and shaded individuals vacuoles in response to higher temperatures (Friemert et al., 1988;

◦

of this species (more than 3 C). Overall, the sun-exposed indi- Behzadipour et al., 1998; Savchenko et al., 2002; Lin et al., 2006),

viduals of A. nudicaulis showed similar values to Vriesea species. avoiding acid leakage during a warming event. On the other hand,

Regarding these differences in A. nudicaulis responses, the more in agreement with our observations for V. bituminosa, other stud-

constant conditions along days and years of shade environments ies have also reported daily variations of thermal tolerance in C3

seems to increase and stabilize (i.e. reduce the plasticity) the ther- plants (e.g., Braun et al., 2002; Froux et al., 2004; Campos, 2011).

mal tolerance of this species. These results are consistent with the This variation may be related to changes in sun-exposure or leaf

ﬁndings that light conditions interact strongly with heat stress temperature throughout the day (Braun et al., 2002; Froux et al.,

and can, at high intensity, damage the photosynthetic appara- 2004), or may even be due to sensitivity to the water stress experi-

tus (Valladares and Pearcy, 1997; but see Krause et al., 2016). On enced at the hottest time of day during the dry season (see Goltsev

the other hand, since A. nudicaulis is from Bromelioideae and V. et al., 2012; Rollins et al., 2013; Zivcak et al., 2013; Zivcak et al.,

minarum and V. bituminosa are from Tillandsioideae subfamily, the 2014).

similar thermal tolerance observed among the last two species may Heat tolerance was a very important variable for distinguishing

be explained not only by the inﬂuence of their photosynthetic path- the ecological strategies of the studied groups. Thus, this parameter

way (i.e. C3 photosynthesis), but also by a phylogenetic signal, as could be used as a trait to differentiate the functional roles of plants.

shown by Marques et al. (2012) and Müller et al. (2016) for seed Furthermore, the strong correlation between both assays of heat

germination of bromeliads. tolerance demonstrated that the studied bromeliads do not have

The low plasticity of heat tolerance found for all studied groups the thermal trade-off described for animals by Rezende et al. (2014).

in this study (RDPI < 0.04) corroborated the ﬁndings of Araújo et al. That is, the most tolerant bromeliad species to increasing temper-

(2013), which show that plants often exhibit low variability in heat ature was also the one able to withstand stressful temperatures for

tolerance. The authors suggest that this is a consequence of the lim- longer periods. This lack of thermal trade-off may be common in

ited variation in the ability of organisms to avoid the destabilizing plants, since their physiological strategies are distinct from those

effects of elevated temperatures on membranes and proteins, since of animals; or it may be a consequence of the pronounced daily and

the changes in lipid composition of membranes and the increased annual temperature variation in campo rupestre formations (see

production of heat shock proteins are normally not enough to Alves et al., 2014; Silveira et al., 2016).

◦

enable them to deal with temperatures above 45 C. Thus, despite Our results showed that bromeliads’ ability to overcome hot

being small, the observed differences in T50 plasticity among tested temperatures, together with its plasticity, may be relevant for

groups are ecologically relevant for campo rupestre bromeliads. explaining their current distribution. In this case, the species cur-

Among the few studies providing estimates of photosynthetic rently restricted to the inter-glacial refuge (i.e. campo rupestre),

heat tolerance in CAM plants, Weng and Lai (2005) — who assessed may be more threatened by climate changes due to their lower

the temperature at which the minimal ﬂuorescence (F0) starts to heat tolerance and plasticity. Our study also indicated that CAM

increase sharply (Tc) — found that the CAM bromeliad Ananas como- bromeliads may potentially be more heat tolerant than C3 plants,

sus showed greater heat tolerance than some C3 and C4 species. In but their heat tolerance and its plasticity are highly affected by

another study comparing the same species to other C3 species, A. sun exposure conditions and climate seasonality. Furthermore, our

comosus was again the most heat tolerant (Yamada et al., 1996). results also indicated that heat tolerance, especially the ability

Transforming the Tc values obtained by Weng and Lai (2005) into to withstand stressful temperatures for a long time, is an impor-

T50, using the equations provided by Knight and Ackerly (2003), tant parameter that differentiates the ecological strategies of these

◦

we obtained a T50 close to 49.5 C for A. comosus. This value is quite bromeliads species. This is the ﬁrst case study evaluating the

similar to the greatest T50 values observed for A. nudicaulis, in the ability of campo rupestre species to overcome warming tempera-

◦

current study (T50 = 50.8 C), and to previously published values of tures. Further investigation on this topic will certainly improve our

C3 species from a hot Californian desert in USA (Knight and Ackerly, understanding about the effects of climate change on this megadi-

2002). In another study, based on a T50-like index for electrolyte verse ecosystem.

leakage, Didden-Zopfy and Nobel (1982) show that the CAM cactus

Opuntia bigelovii, from the same Californian desert, had a T50-like

index similar to the greatest values recorded by Knight and Ackerly

◦

(2002) (closed to 60 C). In summary, although A. comosus and A.

nudicaulis did not usually experience such high temperatures, they Acknowledgment

showed a heat tolerance similar to that of most C3 plants native

This work was supported by CNPq (Conselho Nacional de Desen-

to this desert. Therefore, it is likely that CAM plants are essentially

volvimento Cientíﬁco e Tecnológico) and FAPEMIG (Fundac¸ ão de

more capable of tolerating increasing temperatures, but their heat

Amparo à Pesquisa do Estado de Minas Gerais) Brazilian foun-

tolerance can be diminished by other environmental stresses such

dations.. We thank CAPES (Coordenac¸ ão de Aperfeic¸ oamento de

as sun exposure. Furthermore, the assumed greater heat tolerance

Pessoal de Nível Superior) for the scholarship awarded to CJNC;

of CAM plants, together with their water conservative mechanism,

Santuário Nossa Senhora da Piedade staff for the research permis-

agree with previous assumptions that global increase in average

sions and the pleasant stay during the ﬁeld work; and Vincenzo

temperature and arid areas may favor these plants (e.g. Graham

Ellis, Megan King and Felipe Aoki for the English review. We also

and Nobel, 1996; Reyes-García and Andrade, 2009).

thank the anonymous reviewers of Flora journal for their insightful

The negative relationship between heat tolerance and titratable

comments and suggestions.

acidity of shaded and sun-exposed A. nudicaulis was reﬂected in the

C.J.N. Chaves et al. / Flora 238 (2018) 110–118 117

Appendix A. Supplementary data B.K., Luther, H., Till, W., Zizka, G., Berry, P.E., Sytsma, K.J., 2014. Adaptive

radiation, correlated and contingent evolution: and net species diversiﬁcation

in Bromeliaceae. Mol. Phy. Evol. 71, 55–78.

Supplementary data associated with this article can be found,

Givnish, T.J., 2015. Adaptive radiation versus radiation and explosive

in the online version, at http://dx.doi.org/10.1016/j.ﬂora.2017.05. diversiﬁcation: why conceptual distinctions are fundamental to understanding

003. evolution. New Phytol. 207, 297–303.

Godoy, O., de Lemos-Filho, J.P., Valladares, F., 2011. Invasive species can handle

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